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Live Birth in an Archosauromorph Reptile

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Live Birth in an Archosauromorph Reptile ARTICLE Received 8 Sep 2016 | Accepted 30 Dec 2016 | Published 14 Feb 2017 DOI: 10.1038/ncomms14445 OPEN Live birth in an archosauromorph reptile Jun Liu1,2,3, Chris L. Organ4, Michael J. Benton5, Matthew C. Brandley6 & Jonathan C. Aitchison7 Live birth has evolved many times independently in vertebrates, such as mammals and diverse groups of lizards and snakes. However, live birth is unknown in the major clade Archosauromorpha, a group that first evolved some 260 million years ago and is represented today by birds and crocodilians. Here we report the discovery of a pregnant long-necked marine reptile (Dinocephalosaurus) from the Middle Triassic (B245 million years ago) of southwest China showing live birth in archosauromorphs. Our discovery pushes back evidence of reproductive biology in the clade by roughly 50 million years, and shows that there is no fundamental reason that archosauromorphs could not achieve live birth. Our phylogenetic models indicate that Dinocephalosaurus determined the sex of their offspring by sex chromosomes rather than by environmental temperature like crocodilians. Our results provide crucial evidence for genotypic sex determination facilitating land-water transitions in amniotes. 1 School of Resources and Environmental Engineering, Hefei University of Technology, Hefei 230009, China. 2 Chengdu Center, China Geological Survey, Chengdu 610081, China. 3 State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Palaeontology, CAS, Nanjing 210008, China. 4 Department of Earth Sciences, Montana State University, Bozeman, Montana 59717, USA. 5 School of Earth Sciences, University of Bristol, Bristol BS8 1RJ, UK. 6 School of Life and Environmental Sciences, The University of Sydney, Sydney, New South Wales 2006, Australia. 7 School of Earth and Environmental Sciences, University of Queensland, Brisbane, Queensland 4072, Australia. Correspondence and requests for materials should be addressed to J.L. (email: [email protected]). NATURE COMMUNICATIONS | 8:14445 | DOI: 10.1038/ncomms14445 | www.nature.com/naturecommunications 1 ARTICLE NATURE COMMUNICATIONS | DOI: 10.1038/ncomms14445 daptations related to reproduction directly affect two other major lineages, Testudines (turtles) and the ability of organisms to produce subsequent genera- Archosauromorpha. Ations and persist over evolutionary time scales1. Basal archosauromorph reptiles first appeared in the The evolutionary transition from egg-laying (oviparity) to live Late Permian and diversified in the Triassic18. They birth (viviparity) involves subtle changes to maternal include trilophosaurs, protorosaurs, rhynchosaurs and morphology, physiology, and behaviour, which can lead to archosauriforms, the latter of which includes the ancestors matrotrophy (feeding by the mother, for example through a of the crown-group, namely the birds and crocodilians, and placenta) and shifts in ecological and evolutionary trajectories1–3. their extinct relatives including non-avian dinosaurs and Despite the complexity of this transition, viviparity has evolved pterosaurs among others18. All crown-group archosauromorphs at least 115 times in extant squamates (lizards and snakes), in lay calcified eggs19, the fossil record of which can be traced addition to a single time in the common ancestor of therian back at least to the Early Jurassic20,21. However, the repro- mammals2,4. Moreover, viviparity is a common reproductive ductive biology of stem-group archosauromorphs remains mode in extinct aquatic reptiles5 including eosauropterygians6,7, unknown. ichthyosaurs8–12, mosasauroids13,14, some choristoderans15 Here we report a new specimen of the aquatic protorosaur and likely mesosaurs16,17. However, all of the above viviparous Dinocephalosaurus22 from the Middle Triassic of South China reptile lineages are concentrated within one of the three major containing an embryo in the abdominal region. The pregnant lineages of extant reptiles—the Lepidosauromorpha—plus specimen provides evidence of live birth in a reptile with some completely extinct aquatic groups with uncertain affinities undoubted archosauromorph affinity and insight into the (Fig. 1). No evidence for viviparity has been discovered in the reproductive biology of stem-group archosauromorphs. Time scale creator 2012 chart (O/V) (O) Ma Period Lepidosauromorpha Crocodylomorpha (O) Monotremata (O) Dinosauria (including birds) (O) Testudines (V) Theria Quaternary Neogene (O/V) Choristodera 20 40 Paleogene (V) Eosauropterygia 60 (O) Pterosauria 80 (V) Ichthyopterygia 100 Cretaceous 120 140 160 Jurassic Mammalia 180 200 220 Triassic Dinocephalosaurus 240 (V) 260 ( Archosauromorpha (? V) Mesosauridae Permian 280 300 ( Reptilia 320 Amniota 340 Carboniferous Figure 1 | Evolution of reproductive modes in major groups of amniotes. The phylogenetic tree is derived from a combination of published sources18,45. O, egg-laying (oviparous); V, live-bearing (viviparous). 2 NATURE COMMUNICATIONS | 8:14445 | DOI: 10.1038/ncomms14445 | www.nature.com/naturecommunications NATURE COMMUNICATIONS | DOI: 10.1038/ncomms14445 ARTICLE a b 100° 105° 110° 115° 120° Weining Formation Beds Age Lithology Liupanshui 30° YT Calcareous 146 mudstone South China Block KD Guizhou SF 25° Muddy Yunnan limestone NP Anshun Thick 26° 20° Panxian limestone Guanling Limestone Fuyuan with bitumen Bentonite conodont zone) Qujing Yangtze Platform Zhenfeng 75-145 Siliceous Xingyi limestone Kunming Luoping Dolomitic limestone Nicoraella kockeli Longlin Lamellar/thin Khamdian Massif limestone Luxi Nanpanjiang Basin Nodular limestone 69-74 Member II of Guanling Fm.(part) Guangnan Bioclastic 24° limestone 102° 104° 106° Sandy Uplifted area Tidal flat Open-water basin limestone Micritic limestone Pelsonian, Anisian, Middle Triassic ( Islands Intraplatform basin Restricted platform 8-68 Sutures/faults YT Yangtze Platform KD Khamdian Massif NP Nanpanjiang Basin SF South China Fold Belt Fossil locality 1-7 Figure 2 | Locality and horizon of the new Dinocephalosaurus specimen LPV 30280. (a) Paleotectonic map showing the location of the Luoping biota where LPV 30280 is preserved23. Scale bar, 60 km. (b) Stratigraphic column of the Dawazi section23 showing the horizon of LPV 30280. Scale bar, 2 m. Results a remarkably elongated neck formed by an increased number Geological background. The new specimen belongs to of cervical vertebrate, free sacral and caudal ribs from the recently discovered Luoping biota23,24, which is preserved relevant vertebrae, round tarsus ossifications and moderate in an intraplatform basin of the Yangtze Platform in the South hyperphalangy in the pes. These distinct synapomorphies make China Block (Fig. 2a). Conodont analysis dates the biota to the the identification of the new material as Dinocephalosaurus Pelsonian substage of the Anisian in the Middle Triassic25, unambiguous. Slight differences exist, but currently the available corresponding to an age of B244–245 million years ago (Ma). specimens are not enough to reach a firm conclusion that these The Luoping biota comprises thousands of extremely well differences are stable between specimens from two different preserved fossil specimens23,24. The specimen was collected in locations (see Supplementary Note 1 for detailed description 2008 from Bed 74 of the Dawazi section (Fig. 2b) in Luoping of the specimen). Using both parsimony and Bayesian County, Yunnan Province, China. The thin micritic limestone methods, phylogenetic analyses incorporating all well-known layer bearing the specimen immediately overlies a set of thick- protorosaurian genera reveal a closer phylogenetic relationship bedded siliceous nodular limestones (Fig. 2b). Before collection, of Dinocephalosaurus to the derived tanystropheids than to the specimen had already been weathered into three blocks in other protorosaurs (Fig. 4; Supplementary Figs 1 and 2). the field, the fractures of which were filled with modern soils. The specimen was then transferred from Luoping to the Chengdu Center of China Geological Survey for routine Description of the embryo. The embryo preserved in specimen mechanical preparation. LPV 30280 contains several pieces of mostly articulated cervical vertebrae associated with cervical ribs, part of the forelimbs and pieces of other unidentifiable elements (Fig. 3c,d). Systematic palaeontology and phylogenetic analysis. The It clearly belongs to the same species as the adult, as indicated Luoping specimen (Fig. 3) is catalogued as LPV 30280 in by the shared morphology, including greatly elongated cervical the Chengdu Center of China Geological Survey. It shares vertebrae, very low cervical neural spines and elongated several unequivocally derived characters with published cervical ribs extending across at least three intervertebral articu- Dinocephalosaurus specimens among protorosaurs, including lations. The identification of this embryo as Dinocephalosaurus is NATURE COMMUNICATIONS | 8:14445 | DOI: 10.1038/ncomms14445 | www.nature.com/naturecommunications 3 ARTICLE NATURE COMMUNICATIONS | DOI: 10.1038/ncomms14445 a c e 10 cm 10 cm b d ra cv crh h f cv h cv crh ul prz cv poz ax m crh fe ti car fi ha mt5 mt1 d4 f Figure 3 | Skeleton of the new Dinocephalosaurus specimen LPV 30280. (a) Photograph. The three separate blocks are arranged following their original positions in the field. (b) Interpretive drawing. Dotted line indicates the rough course of the vertebral column of the adult. The different colour in the cervical region aims to facilitate the association of cervical ribs with
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